Adaptive strategies for reading with a forced retinal location.

Forcing normal-sighted participants to use a distinct parafoveal retinal location for reading, we studied which part of the visual field is best suited to take over functions of the fovea during early stages of macular degeneration (MD). A region to the right of fixation lead to best reading performance and most natural gaze behavior, whereas reading performance was severely impaired when a region to the left or below fixation had to be used. An analysis of the underlying oculomotor behavior revealed that practice effects were accompanied by a larger number of saccades in text direction and decreased fixation durations, whereas no adjustment of saccade amplitudes was observed. We provide an explanation for the observed performance differences at different retinal locations based on the interplay of attention and eye movements. Our findings have important implications for the development of training methods for MD patients targeted at reading, suggesting that it would be beneficial for MD patients to use a region to the right of their central scotoma.

[1]  D. Sparks,et al.  Population coding of the direction, amplitude, and velocity of saccadic eye movements by neurons in the superior colliculus. , 1990, Cold Spring Harbor symposia on quantitative biology.

[2]  G. Legge,et al.  Functional and cortical adaptations to central vision loss , 2005, Visual Neuroscience.

[3]  A. Leventhal,et al.  Signal timing across the macaque visual system. , 1998, Journal of neurophysiology.

[4]  S. Trauzettel-Klosinski,et al.  Eye movements in reading with hemianopic field defects: the significance of clinical parameters , 1998, Graefe's Archive for Clinical and Experimental Ophthalmology.

[5]  M. Morrone,et al.  Extraretinal Control of Saccadic Suppression , 2000, The Journal of Neuroscience.

[6]  Robert W Massof,et al.  Is there a standard of care for eccentric viewing training? , 2004, Journal of rehabilitation research and development.

[7]  B. Dosher,et al.  The role of attention in the programming of saccades , 1995, Vision Research.

[8]  L. Arend,et al.  Reading with a macular scotoma. I. Retinal location of scotoma and fixation area. , 1986, Investigative ophthalmology & visual science.

[9]  R A Schuchard,et al.  Relative locations of macular scotomas near the PRL: effect on low vision reading. , 1999, Journal of rehabilitation research and development.

[10]  Daniel Guitton,et al.  Superior colliculus encodes distance to target, not saccade amplitude, in multi-step gaze shifts , 2003, Nature Neuroscience.

[11]  J. Hoffman,et al.  The role of visual attention in saccadic eye movements , 1995, Perception & psychophysics.

[12]  R. E. Morrison,et al.  Manipulation of stimulus onset delay in reading: evidence for parallel programming of saccades. , 1984, Journal of experimental psychology. Human perception and performance.

[13]  E. Faye,et al.  Clinical Low Vision , 1976 .

[14]  J. H. Bertera,et al.  The availability of useful information to the right of fixation in reading , 1982, Perception & psychophysics.

[15]  M Mackeben,et al.  The importance of sustained attention for patients with maculopathies , 2000, Vision Research.

[16]  K L Petre,et al.  Reading with Eccentric Fixation is Faster in Inferior Visual Field Than in Left Visual Field , 2000, Optometry and vision science : official publication of the American Academy of Optometry.

[17]  C. Curcio,et al.  Topography of ganglion cells in human retina , 1990, The Journal of comparative neurology.

[18]  Jeremy Nathans,et al.  Macular degeneration: recent advances and therapeutic opportunities , 2006, Nature Reviews Neuroscience.

[19]  J. Henderson,et al.  Effects of foveal processing difficulty on the perceptual span in reading: implications for attention and eye movement control. , 1990, Journal of experimental psychology. Learning, memory, and cognition.

[20]  Erik D. Reichle,et al.  Toward a model of eye movement control in reading. , 1998, Psychological review.

[21]  J. O'regan,et al.  Is there a systematic location for the pseudo-fovea in patients with central scotoma? , 1993, Vision Research.

[22]  K. Rayner Eye movements in reading and information processing: 20 years of research. , 1998, Psychological bulletin.

[23]  K. Nakayama,et al.  Sustained and transient components of focal visual attention , 1989, Vision Research.

[24]  M Mackeben,et al.  Sustained focal attention and peripheral letter recognition. , 1999, Spatial vision.

[25]  C. Frennesson,et al.  Patients with AMD and a large absolute central scotoma can be trained successfully to use eccentric viewing, as demonstrated in a scanning laser ophthalmoscope , 2003, Vision Research.

[26]  V. Lamme,et al.  The distinct modes of vision offered by feedforward and recurrent processing , 2000, Trends in Neurosciences.

[27]  P. Jong Prevalence of age-related macular degeneration in the United States. , 2004 .

[28]  A. Safran,et al.  Development of a viewing strategy during adaptation to an artificial central scotoma , 2004, Vision Research.

[29]  G. Rizzolatti,et al.  Reorienting attention across the horizontal and vertical meridians: Evidence in favor of a premotor theory of attention , 1987, Neuropsychologia.

[30]  C. Galletti,et al.  The cortical visual area V6: brain location and visual topography , 1999, The European journal of neuroscience.

[31]  J. Schwarzbach Priming of eye movements by masked stimuli , 1999 .

[32]  Susanne Trauzettel-Klosinski,et al.  Fixation behavior and reading ability in macular scotoma: Assessed by Tuebingen manual perimetry and scanning laser ophthalmoscopy , 1996 .

[33]  R. Schuchard,et al.  Preferred retinal loci relationship to macular scotomas in a low-vision population. , 1997, Ophthalmology.

[34]  Benita J. O’Colmain,et al.  Prevalence of age-related macular degeneration in the United States. , 2004, Archives of ophthalmology.

[35]  John H. R. Maunsell,et al.  The visual field representation in striate cortex of the macaque monkey: Asymmetries, anisotropies, and individual variability , 1984, Vision Research.

[36]  G. Rubin,et al.  Fixation patterns and reading rates in eyes with central scotomas from advanced atrophic age-related macular degeneration and Stargardt disease. , 1996, Ophthalmology.

[37]  M. Corbetta,et al.  A Common Network of Functional Areas for Attention and Eye Movements , 1998, Neuron.

[38]  J. H. Bertera The effect of simulated scotomas on visual search in normal subjects. , 1988, Investigative ophthalmology & visual science.

[39]  John H. R. Maunsell,et al.  Visual response latencies in striate cortex of the macaque monkey. , 1992, Journal of neurophysiology.

[40]  Timothy McMahon,et al.  Eye-movement training for reading in patients with age-related macular degeneration. , 2005, Investigative ophthalmology & visual science.

[41]  K. Rayner,et al.  Eye movements during reading: some current controversies , 2001, Trends in Cognitive Sciences.

[42]  Benjamin Rappaz,et al.  Processes involved in oculomotor adaptation to eccentric reading. , 2006, Investigative ophthalmology & visual science.

[43]  Ralph Radach,et al.  The Role of Attention and Spatial Selection in Fluent Reading , 2002 .

[44]  Gary S Rubin,et al.  Reading with simulated scotomas: attending to the right is better than attending to the left , 1999, Vision Research.

[45]  E Peli,et al.  Control of eye movement with peripheral vision: implications for training of eccentric viewing. , 1986, American journal of optometry and physiological optics.

[46]  G. Rizzolatti,et al.  Space and selective attention , 1994 .

[47]  S. Yantis,et al.  Transient neural activity in human parietal cortex during spatial attention shifts , 2002, Nature Neuroscience.

[48]  D. Spinelli,et al.  Eye Movement Patterns in Reading as a Function of Visual Field Defects and Contrast Sensitivity Loss , 1996, Cortex.

[49]  R. Wilcox Introduction to Robust Estimation and Hypothesis Testing , 1997 .

[50]  R. Wurtz,et al.  Saccade-related activity in monkey superior colliculus. I. Characteristics of burst and buildup cells. , 1995, Journal of neurophysiology.

[51]  K. Rayner,et al.  Asymmetry of the effective visual field in reading , 1980, Perception & psychophysics.

[52]  H. Bedell,et al.  The oculomotor reference in humans with bilateral macular disease. , 1990, Investigative ophthalmology & visual science.

[53]  Stephen J. Heinen,et al.  Adaptation of saccades and fixation to bilateral foveal lesions in adult monkey , 1992, Vision Research.

[54]  P. Cavanagh,et al.  Attentional resolution and the locus of visual awareness , 1996, Nature.

[55]  J. G. Strong,et al.  Demographic characteristics of the vision-disabled elderly. , 1997, Investigative ophthalmology & visual science.

[56]  Jens Schwarzbach,et al.  Response priming with and without awareness , 2006 .

[57]  H. Deubel,et al.  Saccade target selection and object recognition: Evidence for a common attentional mechanism , 1996, Vision Research.